ABSTRACT 1. Recent theory suggests that compensation or even overcompensation in stage-specific biomass can arise in response to increased mortality. Which stage that will show compensation depends on whether maturation or reproduction is the more limiting process in the population. Size-structured theory also provides a strong link between the type of regulation and the expected population dynamics as both depend on size/stage-specific competitive ability. 2. We imposed a size-independent mortality on a consumer-resource system with Daphnia pulex feeding on Scenedesmus obtusiusculus to asses the compensatory responses in Daphnia populations. We also extended an existing stage-structured biomass model by including several juvenile stages to test whether this extension affected the qualitative results of the existing model. 3. We found complete compensation in juvenile biomass and total population fecundity in response to harvesting. The compensation in fecundity was caused by both a higher proportion of fecund females and a larger clutch size under increased mortality. We did not detect any difference in resource levels between treatments. 4. The model results showed that both stages of juveniles have to be superior to adults in terms of resource competition for the compensatory response to take place in juvenile biomass. 5. The results are all in correspondence with that the regulating process within the population was reproduction. From this, we also conclude that juveniles were superior competitors to adults, which has implications for population dynamics and the kind of cohort cycles seen in Daphnia populations. 6. The compensatory responses demonstrated in this experiment have major implications for community dynamics and are potentially present in any organisms with food-dependent growth or development.

[Show abstract][Hide abstract]ABSTRACT:
Ontogenetic development is a fundamental aspect of the life history of all organisms and has major effects on population and community dynamics. We postulate a general conceptual framework for understanding these effects and claim that two potential energetics bottlenecks at the level of the individual organism--the rate by which it develops and the rate by which it reproduces--form a fundamental route to symmetry-breaking in ecological systems, leading to ontogenetic asymmetry in energetics. Unstructured ecological theory, which ignores ontogenetic development, corresponds to a limiting case only, in which mass-specific rates of biomass production through somatic growth and reproduction, and biomass loss through mortality, are independent of body size (ontogenetic symmetry). Ontogenetic symmetry results in development and reproduction being limited to the same extent by food density. In all other cases, symmetry-breaking occurs. Ontogenetic asymmetry results in increases in juvenile, adult, or even total biomass in response to mortality. At the community level, this gives rise to alternative stable states via predator-induced shifts in prey size distributions. Ontogenetic asymmetry furthermore leads to two distinct types of cycles in population dynamics, depending on whether development or reproduction is most energy limited. We discuss the mechanisms giving rise to these phenomena and the empirical support for them. We conclude that the concepts of ontogenetic symmetry and ontogenetic asymmetry form a novel and general organizing principle on which future ecological theory should be developed.

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Experimental and theoretical studies show that mortality imposed on a population can counter-intuitively increase the density of a specific life-history stage or total population density. Understanding positive population-level effects of mortality is advancing, illuminating implications for population, community, and applied ecology. Reconciling theory and data, we found that the mathematical models used to study mortality effects vary in the effects predicted and mechanisms proposed. Experiments predominantly demonstrate stage-specific density increases in response to mortality. We argue that the empirical evidence supports theory based on stage-structured population models but not on unstructured models. We conclude that stage-specific positive mortality effects are likely to be common in nature and that accounting for within-population individual variation is essential for developing ecological theory.

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CompletecompensationinDaphniafecundityandstage-specificbiomassinresponsetosize-independentmortalityKarinA.Nilsson1*,LennartPersson1andTobiasvanKooten1,21DepartmentofEcologyandEnvironmentalScience,Umea ˚ University,S-90187Umea ˚,Sweden;and2WageningenIMARES,POBox68,1970ABIJmuiden,theNetherlandsSummary1. Recent theory suggests that compensation or even overcompensation in stage-specific biomasscan arise in response to increased mortality. Which stage that will show compensation depends onwhether maturationor reproductionisthemorelimitingprocessinthepopulation.Size-structuredtheory also provides a strong link between the type of regulation and the expected populationdynamicsasbothdependonsize⁄stage-specificcompetitiveability.2. We imposed a size-independent mortality on a consumer-resource system with Daphnia pulexfeedingonScenedesmusobtusiusculustoassesthecompensatoryresponsesinDaphniapopulations.We also extended an existing stage-structured biomass model by including several juvenile stagestotestwhetherthisextensionaffectedthequalitativeresultsoftheexistingmodel.3. We found complete compensation in juvenile biomass and total population fecundity inresponse to harvesting. The compensation in fecundity was caused by both a higher proportion offecund females and a larger clutch size under increased mortality. We did not detect any differenceinresourcelevelsbetweentreatments.4. The model results showed that both stages of juveniles have to be superior to adults in terms ofresourcecompetitionforthecompensatoryresponsetotakeplaceinjuvenilebiomass.5. The results are all in correspondence with that the regulating process within the population wasreproduction. From this, we also conclude that juveniles were superior competitors to adults,whichhasimplicationsforpopulationdynamicsandthekindofcohortcyclesseeninDaphniapop-ulations.6. Thecompensatoryresponsesdemonstratedinthisexperimenthavemajorimplicationsforcom-munity dynamics and are potentially present in any organisms with food-dependent growth ordevelopment.Key-words: biomass compensation, biomass model, compensatory response, Daphnia pulex,harvesting, population dynamics,populationregulation,regulatory mechanisms, size dependence,stagestructureIntroductionCompensatory responses in rates or processes in ecologicalsystemshavebeenthefocusofmanystudies.Theoverwhelm-ing majority of these studies have been concerned with com-pensation in individual growth and fecundity (Metcalfe &Monaghan 2001) and has been documented for differentkinds of organisms ranging from fish (Nicieza & Metcalfe1997) and amphibians (Wilbur1988) to plants (Hawkes &Sullivan 2001; Callaway, Pennings & Richards 2003). Suchcompensation can occur in response to different factors. Forexample, an increased mortality on a consumer populationwill result in a release of resource competition that, in turn,increases individual growth or fecundity in the consumerpopulation(Wilbur1988).Overall,theabovestudieshavebeenrestrictedtoresponsesin per capita rates. In contrast, recent theoretical insightsshow that compensation or even overcompensation in stage-specific biomass can arise in response to increased mortality.The theoretical understanding of the emergence of stage-spe-cific overcompensation is based on that two processes, matu-ration orreproduction,canberegulatingwithin apopulation*Correspondenceauthor.E-mail:karin.nilsson@emg.umu.seJournalofAnimalEcology2010,79,871–878doi:10.1111/j.1365-2656.2010.01679.x?2010TheAuthors.Journalcompilation?2010BritishEcologicalSociety

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(de Roos et al. 2007). When maturation is more regulating,an increase in mortality increases the maturation rate leadingto an increase in adult biomass. In contrast, when reproduc-tion is more regulating, the biomass compensation takesplace in the juvenile stage through an increase in reproduc-tion rate (de Roos et al. 2007). Experimental studies havereportedthepresenceofstage-specificovercompensationasaresponse to size-selective mortality in a variety of organisms,such as water fleas, blowflies, flour beetles and fish, (Watt1955; Slobodkin & Richman 1956; Nicholson 1957; Edley &Law 1988; Moe, Stenseth & Smith 2002; Cameron & Benton2004; Schro ¨ der, Persson & de Roos 2009). Although theseexperimental studies concerned size-selective mortality, the-ory predicts that overcompensation is also possible with ran-dommortality(deRooset al.2007).Stage-specific compensatory responses in biomass havemajor ramifications for community dynamics (de Roos &Persson 2002). For example, an emergent Allee effect canoccur, when the feeding of a size-selective predator inducesovercompensation in the targeted size class of its prey (deRoos & Persson 2002; Persson et al. 2007). This leads to thepresence of alternative stable states, and increases the risk ofcatastrophic collapse of the predator population such as hasbeen observed in the North West Atlantic cod (Frank et al.2005; VanLeeuwen,DeRoos& Persson 2008). Anotherphe-nomenon is emergent facilitation, where a size-selective pred-ator induces overcompensation in a stage of its prey which ispreyed upon by another predator species. The first predatorthen facilitates and is essential for the existence of the otherby changing the size structure of the prey population (deRooset al.2008a).Maturation or reproduction regulation is related to stage-specific ecological performance, and depends on the relativecompetitive strength of individuals in different life stages. (deRoos et al. 2007). A link thereby exists between the type ofpopulation regulation and consumer-resource dynamics insize-structured populations, as the type of dynamics exhib-ited by a population also largely depends on the competitivehierarchy of differently sized individuals (de Roos & Persson2003; de Roos et al. 2008b). In Daphnia, small amplitudecohort cycles have been observed, the nature of which hasbeen the source of substantial discussion (Murdoch &McCauley1985;McCauleyet al.1999).Ithasbeensuggestedthat the smallest juveniles are superior competitors and thatthe cohort cycles seen in Daphnia populations are driven byfecunditysuppressionbydominantjuvenilecohorts(deRooset al. 1990; McCauley et al. 1999). Individual level experi-ments, on the other hand, have indicated that intermediatelysized individuals are superior (Gurney et al. 1990; de Rooset al. 1997). Results from recent studies have also suggestedthat the adults may have a competitive advantage (McCau-ley,Nelson &Nisbet2008).To address the question about the presence of compensa-tory responses in Daphnia and whether maturation or repro-duction is regulating in Daphnia populations, we carried outan experiment with Daphnia pulex [Leydig 1860] feeding onalgae where we imposed a harvesting mortality on the D. pu-lex. The harvesting was random and size-independent to testwhether compensation was present for random mortality.Basedonexistingmodels(deRooset al.2007)andsize-struc-tured population theory, we predicted that compensation orovercompensation would be present in either the juvenile orthe adultstage. If juveniles are superior competitors to adultsand reproduction is the regulating process in the populationwe expect: (i) compensation or overcompensation in juvenilebiomass, (ii) compensation or overcompensation in totalreproduction, (iii) overall dominance in adult biomass, (iv) ashift in the adult size structure with imposed harvesting. Ifadults are superior competitors to juveniles and maturationis the regulating process in the population we expect thereversed pattern. The results of the harvesting experimentwere also set in relation to mechanisms that have been sug-gested to drive cycles in Daphnia. Finally, we analysed thedynamics of a model of two juvenile and one adult stagesfeeding on a single resource, with Daphnia parameters andsize-independent harvest. This was performed to address thepossibility that intermediately sized individuals may becompetitively superior to both small juveniles and adults andto evaluate if the three-stage model would guild the samequalitative results as the two-stage models (de Roos et al.2007).MaterialsandmethodsEXPERIMENTThe experiment was set up as a semi-chemostat dynamic system in alight and temperature controlled experimental room at Umea ˚ Uni-versity, Sweden. Daphnia pulex was introduced to 12 aerated aquariafilled with 10Æ3 L of tap water. Water containing the algae Scenedes-mus obtusiusculus [Chodat 1913] was pumped into the aquaria at arate of 2 mL per minute resulting in a dilution rate of 0Æ011 h)1. Tomaintain a constant volume intheaquaria,outflowholes, coveredbynets that retained the D. pulex but not the algae, were positioned atthelevelofthewatersurface.Algalinflowwaspumpedfrom12aqua-ria in which the concentration of S. obstusiusculus was adjusted threetimes per week to a concentration of 51 000 cells per mL, corre-sponding to 1 mg carbon and 36Æ5 lg chl a per litre. Algae wereobtained bykeeping monoculturesofS.obstusiusculusinbottlescon-taining H2S medium. To adjust the density in the algal inflow aqua-ria, the content of 2–4 bottles was centrifuged at 1000 g for 3 minand the growth medium was decanted, the algal concentration wasthen estimated and the algal water was diluted to obtain the correctalgalconcentration.Thewater temperaturewas20Æ5–22Æ5 ?Candthelight was provided by 80 W fluorescent fixtures providing a photo-synthetic radiation of 26 lE S)1m)2kept on during 24 h per day.Daphnia pulex, originating from the Max Planck Institute for Lim-nologyinPlo ¨ n,wasaddedtotheaquariaonthefirstdayoftheexper-iment and for the following 6 days. The induced mortality wasapplied to half of the D. pulex populations three times per week.Water in the experimental aquaria was mixed for 15–20 s and a vol-ume of 3Æ40 or 4Æ05 L (depending on day) was taken out and filteredthrough a 75 lm mesh net to collect the daphnids, whereafter thewater was returned. This treatment corresponds to an instantaneousmortality of 0Æ2 day. During the experiment, some Drosophila larvaeand chironomids were found in the aquaria and some periphytongrowth on the walls was also noted. No male D. pulex was found.872K.A.Nilsson,L.Persson&T.vanKooten?2010TheAuthors.Journalcompilation?2010BritishEcologicalSociety,JournalofAnimalEcology,79,871–878

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The12D.pulexpopulationsweresampled twiceperweek.Aftermix-ingthewater,asampleof200or400 mLwastakenout.Alldaphnidswerecountedandaminimumof60individuals ineverysample(ifthesample was not smaller than that) were measured to the nearest0Æ04 mm with the help of a stereo microscope. Individuals exceeding1Æ4 mm in length were classified as adults, and as juveniles otherwise(McCauleyet al.1999).Eggsand youngstillinthebroodpouchwerecounted, as well as resting eggs (ephippia) both in the brood pouchand freely floating. The whole sample was returned to the sourceaquarium afterwards. The biomass of D. pulex was calculated usingweight-length relationships [weight in lg = 1Æ59 · (length inmm)2Æ77] from Bottrell et al. (1976). Phytoplankton was sampledtwice a week. A total of 50 mL of water was taken out from the mid-dle of the water column and filteredthrougha 75 lm mesh. Anycap-tured daphnids were returned to the aquaria. The samples werefiltered through a glassfiber filter which was then dried and frozenandlateranalysedforchlorophyllacontent.DATA ANALYSISFor the statistical analysis, 21 sampling occasions were used startingfrom the first samplingafter the treatment started until the end of theexperiment. Juveniles still in the brood pouch were treated as eggs inthe data analysis. To assess the size distributions within stages, thebiomass for each 0Æ1 mm size class was first calculated for eachaquarium separately by taking the proportion of the total stage bio-mass (of the juveniles or adult) that each size class represented foreverysamplingoccasion.Theaverageproportionwasthencalculatedand multiplied with the average juvenile or adult biomass over thewholesamplingperiod.Thiswasdonetoavoidbiasesduetofluctuat-ing samplesizes.Analysisofvariance (anova), Analysis of covariance(ancova), t-tests and regressions were performed in spss version 13Æ0for Windows. Statistical significance was taken at a probability levelofP < 0Æ05.MODELTo investigate how the addition of a second juvenile stage affectscompensatory responses and to demonstrate the nature of such aresponse, we used a model which describes the Daphnia populationas a three-stage-structured population feeding on a single resource.The model is derived from a two-stage (juvenile-adult) biomassmodel developed in de Roos et al. (2007). Our aim was to evaluatethe qualitative predictions of the model and particularly investigatethe effects of including a second juvenile stage on the populationequilibrium states and not to make any quantitative comparisonbetween model and experiment. The juvenile stages are assumed toallocate energy to somatic growth whereas adults use all their netenergy (that part of intake which is left after metabolism is paid for)on reproduction. Maturation and reproduction as well as the transi-tion between juvenile stages are all modelled as food-dependent pro-cesses. We varied the parameters qx, the relative competitive abilityofDaphnia in stage x, to study how the intraspecificcompetitive hier-archy affected the nature of regulation and the compensatoryresponse to mortality. The model is described in detail in the Appen-dixS1andTableS1,Supportinginformation.ResultsMODEL RESULTSCompensation and overcompensation in juvenile biomassonly occurred when both juveniles were competitively supe-rior to adults (Fig. 1a, b). All cases where adults were com-petitively superior to at least one of the juvenile stages didresult in a decrease in total juvenile biomass with increasedmortality (Fig. 1c–f). With inferior adults there was also aclear decrease in adult biomass in response to increased mor-00.10.2 0.300.20.40.60.8100.1 0.20.300.20.40.60.8100.10.20.3Mortality, µ00.20.40.60.8100.1 0.20.300.20.40.60.81Biomass ASJJ+SR0 0.10.20.300.20.40.60.810 0.10.20.300.20.40.60.81a: qJ > qS > qAb: qS > qJ > qAc: qA > qJ > qSd: qJ > qA > qSe: qS > qA > qJf: qA > qS > qJFig. 1. Equilibriumdensitiesofthe consumerandresource inthe stage-structuredmodel,inrelationtomortality(J: smalljuvenile consumers,S:large juvenileconsumers,A:adultconsumers,R:resource)The lettersineachplot indicate the competitivedominancehierarchy,withthestron-gest(leftmost) competitorhavingaq-valueof1Æ2,the intermediate 1Æ0andtheweakeststage 0Æ8.Allotherparametersaresettotheirdefaultval-ues(seeAppendixS1).Completecompensation873?2010TheAuthors.Journalcompilation?2010BritishEcologicalSociety,JournalofAnimalEcology,79,871–878

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tality. Adult biomass was only higher than juvenile biomasswhen adults were the worst competitors and the mortalitywas low(Fig. 1).Inconclusion,the predictionsfrom the two-stage model are still valid with a three-stage model and to getcompensation in juvenile biomass the adult stage needs to becompetitively inferior to both small and intermediately sizedjuveniles.EXPERIMENTAL RESULTSNo difference in juvenile D. pulex biomass was foundbetween the mortality treatment and the control (Fig. 2a,Table 1). The populations in the mortality treatment had alower average adult D. pulex biomass compared to the con-trol (Fig. 2b, Table 1). The adult biomass dominated thepopulations in both treatments (Table 1). The same patternwasfoundin the juvenile(averageandstandarddeviationforthe control treatment: 149 ± 28 individuals L)1, mortality:140 ± 29 individuals L)1)and27 individuals L)1,mortality:densities.Therewasatrendinincreasingbiomassofjuvenilesand adults over time in both treatments followed by adecrease in adult biomass during the later part of the experi-ment. Between treatment differences among juveniles variedover time whereas that of adults increased over time(Table 1). No difference in chlorophyll level was foundbetween treatments. There was also a trend in increasingchlorophylllevelovertime(Fig. 2c,Table 1).There was no difference in total population egg produc-tion between treatments (Fig. 3a, Table 1). The egg produc-tion increased up to day 75 whereafter egg productionstayed relatively constant in both treatments (Fig. 3a). Theadult per capita production of eggs was higher in the mor-tality treatment than in the control and this differenceincreased over time (Fig. 3b, Table 1). The mean clutch sizeof females that had eggs was 4Æ1 in the mortality treatmentand 1Æ9 in the control treatment (t-test; t = )9Æ65,P < 0Æ001, d.f. = 10). The mean proportion of fecundfemales was 0Æ37 in the mortality treatment compared to0Æ27 in the control (t = )2Æ84, P = 0Æ017, d.f. = 10). Thefecundity of the females was also related to their individualsize as an ancova on clutch size with size as a covariate wasalso performed and showed that the interaction term wassignificant (Table 2). Thus, females in the mortality treat-ment did not only have a higher fecundity but the differencebetweentreatments also increasedFigure 4a shows a typical example for clutch size fromtwo aquaria, one control and one mortality treatment. Theinteraction effect in the ancova on the proportion of fecundfemales with size as a covariate showed only a tendency forthat the difference in proportion of fecund females increasedwith female size (Table 2). However, nonlinear regressionon the proportion of fecund females and body size using asigmoid function for each aquarium separately showed thatthe asymptote reflecting the maximum proportion of fecundfemales reached at large sizes was higher in the mortalitytreatment (0Æ92) compared to the control (0Æ65), (t = )4Æ10,P = 0Æ002, d.f. = 10). The average proportion of fecundfemales carrying ephippia was 0Æ15 in the mortality treat-ment and 0Æ13 in the control (t = )1Æ75, P = 0Æ11,d.f. = 10). The ephippia carrying females were not includedin the calculations of proportion fecund females or in thecalculations of total population fecundity or clutch sizes.There was no difference between treatments in biomasssize distribution for the juvenile stage (ancova, Fig. 5a,Table 2). The biomass size distributions were actually verysimilar except for the largest size class of juveniles where thecontrol treatment had a larger average biomass. This differ-ence was however significant when analysed separately(MS = 2885, d.f. = 1, F = 8Æ52, P = 0Æ015). The biomasssize distribution of adults differed between treatments(Table 2). The biomass of the eight largest size classes ofadultswerehowevernotsignificantlydifferentwhenanalysedadult69 ± 12 individuals L)1)(control:171 ±with female size.Juvenile Daphnia biomass (ug L–1) 0100200300400500Adult Daphnia biomass (ug L–1) 010002000300040005000(a)(b)Day20406080100120Chlorophyll level (ug chla L–1) 01234567(c)Fig. 2. Development of juvenile Daphnia biomass (a), adult Daphniabiomass (b) and chlorophyll levels (c) over time. Black circles denotethe mortality treatment and white circles the control treatment(means ± 1 SE). Note that the two-first points are from the B-sideonly and the two last are from the A-side, resulting in 23 samplingdates.874K.A.Nilsson,L.Persson&T.vanKooten?2010TheAuthors.Journalcompilation?2010BritishEcologicalSociety,JournalofAnimalEcology,79,871–878

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separately (Fig. 5b), except for the size class 2Æ5–2Æ6 mmwhere there was a higher biomass in the mortality treatmentcompared to the control treatment (MS = 1Æ081, d.f. = 1,F = 5Æ25,P = 0Æ045).DiscussionNATURE OF REGULATIONWe found a complete compensation in biomass of the juve-nile stage when a substantial size-independent mortality wasimposed. In contrast to Lotka-Volterra type systems, whereonly reproduction regulation is present in a population, mat-uration can also be regulating in a stage-structured popula-tion. The fact that two rates can change and redistribute thebiomass within the population isthe cause behind compensa-tory responses in stage-specific biomass. When reproductionTable 1. Repeated measure analyses of variance of the effects of harvesting on juvenile and adult biomass (lg L)1log (x + 1) transformed),chlorophyll levels (lg chl a L)1, log transformed), total egg production (#L)1, log (x + 1)) transformed and egg production per adult (log(x + 1))transformedbeforeanalysisanovasMortalityaverageControlaverageTreatment Time · treatmentFPFPJuvenileDaphniabiomassAdultDaphniabiomassChlorophylllevelTotaleggproductionEggproductionperadult19465123616730Æ75778Æ90Æ0611Æ50117Æ90Æ405<0Æ000Æ8100Æ249<0Æ002Æ571Æ801Æ111Æ101Æ72<0Æ000Æ0220Æ3380Æ3560Æ0302Æ72Æ81381171Æ50Æ5DayNumber of eggs per female01234Total egg production (# L–1)1101001000(a)(b)2040 6080100120Fig. 3. Development of total egg production (a) and egg productionper adult (b) over time. Black circles denote the mortality treatmentandwhitecirclesthecontroltreatment(means ± 1SD).(a)(b)Fig. 4. Clutch size of fecund Daphnia in relation to female size fromtwo representative aquaria (a), one from the mortality treatment(black circles) and one from the control treatment (white circles).Data from the whole sampling period are included (zero values arenot included). The proportion fecund females with every size class ineach aquarium separate (b). The data set includes all 12 aquaria andthe whole sampling period. Black circles denote the mortality treat-mentandwhitecirclesthecontroltreatment.Table 2. Analyses of covariance of juvenile size distributions (logtransformed), adult size distributions (?x transformed) as well asclutch size (log transformed) and proportion of fecund females(arcsinetransformed)inrelationtofemalesizeancovasTreatmentSize · treatmentFPFPJuvenilesizedistributionAdultsizedistributionClutchsizeProportionfecundfemales2Æ06982Æ2098Æ9961Æ070Æ154<0Æ000Æ0030Æ3021Æ2214Æ1514Æ5072Æ6480Æ297<0Æ00<0Æ000Æ105Completecompensation875?2010TheAuthors.Journalcompilation?2010BritishEcologicalSociety,JournalofAnimalEcology,79,871–878

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is regulating adults are more limited by the resource levelthan juveniles are and the inflow to the juvenile stage (thereproduction rate) is more limited than the outflow of juve-niles (the maturation rate). The inflow to the adult stage willhence be high, which contributes to the accumulation of bio-massinthe adultstage.Withimposednon-size-selectivemor-tality, biomass is removed from both the juvenile and theadult stage. Thetotaladultbiomassbecomes lower, butthereis compensation in biomass in the juvenile stage as the bio-mass inflow to the juvenile stage increases through theincreased reproduction and the juvenile feeding (de Rooset al.2007).Thefact thatthecompensationinbiomassinourexperiment took place in the juvenile stage is in accordancewith that the Daphnia system is reproduction regulated andhence also that juveniles are competitively superior to adults.Thefactthatwefoundcompensationandnotovercompensa-tion in stage-specific biomass can be due to that the magni-tude oftheimposedmortalitycompensatory response in juvenile biomass and populationfecundity exactly matched the loss through harvesting. Mostlikely this was a result of the fact that the mortality weimposed was beyond that where overcompensation occurs. Itshould also be noted that the extent of overcompensation isless pronounced for random mortality (de Roos et al. 2007).Also in correspondence with reproduction regulation, wefound a complete compensation in total population fecun-dity. The compensation resulted from both an increase inclutch size, an individual level mechanism, as well as in theproportion of fecund females, a population level mechanism.In our study, the low number of eggs per adult in both treat-ments, as compared to studies where Daphnia has experi-enced high food concentrations (Gliwicz & Lampert 1994),showed that the egg production was strongly limited by foodavailability inboth control and mortality treatment.Thelackof a mortality effect on phytoplankton biomass in the experi-ment provides further support for that the juveniles are com-petitively superior to the adults. This results from thatjuvenilefeeding largely determines the resource level, hence itis natural that we did not see any trophic cascades in ourresults, with complete compensation in juvenile biomass.Furthermore, the dominance of adult biomass in the controlwassuchthat theis also in accordance with the superior competitive ability ofjuveniles (de Roos et al. 2007). The competitive bottleneck inthe Daphnia populations can be found by a closer inspectionof the size distributions. In terms of biomass, all juvenilestages except for the largest one showed striking similaritiesbetween the two treatments, suggesting that there was no‘stacking’ as a result of reduced growth in the juvenile stage.This pattern indicates that the main difference in competitiveabilities was between juveniles and adults and not amongjuveniles. In contrast, we observed a shift in size structure inthe adult stage suggesting that the competitive bottleneckcould be found here. We did not measure individual growthrate, but we found no difference in biomass in some of thelargest adult size classes and even a higher biomass in one ofthe size classes in the mortality treatment. This indicates fas-ter growth in the mortality treatment, as there was a higherlikelihood of dying in that treatment. Such a response toincreased mortality is also in accordance with reproductionregulation.Previous studies on compensation have used size-selectiveharvesting. Although inconclusive, two previous studies onDaphnia are largely in support of reproduction regulation aswe found (Slobodkin & Richman 1956; Edley & Law 1988).A more complete experiment performed with a poeciliid fishshowed that this population was reproduction regulated asthere was an increase in juvenile biomass in response to bothjuvenile and adult harvesting (Schro ¨ der et al. 2009). Experi-mental studies providing evidence for overcompensation inmaturation regulated systems include soil mites (Cameron &Benton 2004), blowflies (Moe et al. 2002) and flour beetles(Watt 1955). Nicholson’s (1957) classical experiments withblowflies provide a particularly nice example of the relation-ship between the type of overcompensation and which stageis competitively superior as the blowflies’ food was manipu-lated to make either maturation or reproduction limiting.When juveniles received little food, the adult densityincreased with adult harvesting in accordance with matura-tion regulation governed by larval competition. In contrast,when adults received little food, juvenile density increasedwith adult harvest, which is in accordance with reproductionregulationandhighadultcompetition.(a)(b)Fig. 5. Biomass size distribution of juveniles (a) and adults (b) in the controls (white histobars) and harvesting treatment (grey histobars)(means ± 1SD).876 K.A.Nilsson,L.Persson&T.vanKooten?2010TheAuthors.Journalcompilation?2010BritishEcologicalSociety,JournalofAnimalEcology,79,871–878

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MODEL RESULTS AND COMPARISON WITHEXPERIMENTAL DATATheresultsofthethree-stagemodelshowedthesamequalita-tive results in terms of biomass compensation as the two-stage model of de Roos et al. (2007) including the lack ofovercompensation when all stages are equally competitive(see Appendix S1 and Fig. S2, Supporting information). Themain conclusion from extending the two-stage to a three-stage model is that the type of regulation is not determinedby which stage is the best competitor, but by which stage istheworstcompetitor.Inthethree-stagemodel,wefoundthatfor the biomass compensation to take place in the juvenilestage, it did not matter whether the large or small juvenilestage was better as long as both juvenile stages were competi-tivelysuperiortoadults.The experiments were not conducted in darkness, and wehence cannot exclude the possibility that algal productionoccurred within the Daphnia tanks. We analysed a version ofthe model which included this production in addition to thesemi-chemostat resource growth, and found that this doesnot qualitatively affect our results (Appendix S1 and Fig. S1,Supportinginformation).POTENTIAL COMMUNITY EFFECTSBiomass overcompensation is a crucial element in recent the-oretical findings concerning alternative stable states in stage-structured communities. A size-selective predator may pro-mote its own performance by feeding on a prey size classshowing overcompensation (de Roos & Persson 2003). Over-compensation is also a pre-requisite for emergent facilitation(de Roos et al. 2008a), which can occur when a size-selectivepredator induces an increase in another prey size class facili-tating the existence of another predator feeding on that preysize class. As Daphnia is a key grazer in many aquatic sys-tems, it is important to understand how it responds toincreased mortality and the potential effects that this mayhave on food webs. The potential for emergent facilitation isone scenario to be considered. For predators with negativesize selection feeding on small Daphnia (i.e. invertebrate pre-dators), predators feeding on large Daphnia (i.e. vertebratepredators) are not necessarily competitors, but may insteadfacilitate the existence of predators with negative size selec-tion. Compensatory responses in the juvenile Daphnia stageshould be especially pronounced when the regulating stage(i.e. adults) is targeted. There are indications of suchresponses in natural systems, for example, Leibold & Tessier(1991) found a positive correlation between the densities ofpredators with negative and positive size selection in a Daph-niasystem.IMPLICATIONS FOR POPULATION DYNAMICSSize-structured theory provides a strong link between thetype of regulation present in a population and the expectedpopulation dynamics as both depend on size⁄stage-specificcompetitive ability (de Roos & Persson 2003; de Roos et al.2008b). Juvenile driven cohort cycles occur when juvenilesare superior competitors. These cycles are driven by the juve-nile delay per se while the flexibility of the delay is non-essen-tial (de Roos & Persson 2003). This corresponds to areproduction regulated population with relatively constantmaturation rate. In contrast, the flexibility in the juveniledelay is an important mechanism for the presence of adultdriven cycles, which corresponds to maturation regulatedpopulations where adults are superior (de Roos et al. 2008b).Our experimental results are all in correspondence with thatjuveniles are superior competitors, and are hence in favourofjuveniledrivencycles.Many population dynamical experiments have been per-formed on Daphnia-algae systems (Murdoch & McCauley1985; McCauley et al. 1999). According to McCauley &Murdoch (1987), the cohort cycles in Daphnia were driven byjuveniles who suppressed their own growth and adult fecun-dity. In early models and experiments, the smallest juvenileswere also viewed as superior competitors (de Roos et al.1990;McCauleyet al.1999). Incontrast, individualenergeticmodels suggest that small juveniles are inferior to both largejuveniles and adults (Gurney et al. 1990; de Roos et al.1997). In a recent study, McCauley et al. (2008) also providetheoretical and experimental evidence for that Daphniacohort cycles are not juvenile driven cycles but rather havethe period⁄delay ratio of adult driven cycles. Futhermore,the presence of alternative attractors observed in Daphnia(McCauley et al. 1999, 2008) is not expected for logisticresource growth, if the cohort cycles are juvenile driven (deRoos et al. 2008b). At the same time, the Daphnia popula-tions studied by McCauley et al. (2008) were as in our studydominatedby adult biomass which is not expected with adultdrivencycles.In light of these conflicting results, the question may beaddressed whether a compensatory response in juveniles anda dominance of adult biomass and can be reconciled with anadult competitive superiority. First, it may be suggested thatalternative energy-budget models present for Daphnia mayalter the biomass dominance – compensation pattern. How-ever, the major alternative, the Kooijman & Metz (1984)energy-budget model where juveniles pay an energetic costfor building up and maintaining reproductive tissue does notproducethepatternwithadultdominance,nordoescompen-sationinjuvenilesoccur(A.M.deRoos&L.Persson,unpub-lished data). Second, the addition of a second adult stage canbe argued to change predictions. This hypothesis is howeverrejected by the analysis of de Roos et al. (2008a,b) for a four-stage model. Third, we assume equal background mortalityfor juveniles and adults, whereas the model of McCauleyet al.(2008)assumesjuvenilestohaveahighermortalityrate.Still, this change in assumption will anywaynotyield the pat-ternweobservedinourexperiment.In light of that none of the above three alterations canresolve present inconsistencies, it may finally be suggestedthatthecohortcyclesobservedinMcCauleyet al.(2008)rep-resents an alternative juvenile driven cycle described by deCompletecompensation877?2010TheAuthors.Journalcompilation?2010BritishEcologicalSociety,JournalofAnimalEcology,79,871–878